Comprehensive analysis of methods used for the evaluation of compounds against Mycobacterium tuberculosis

Tuberculosis

Volumn 92, Issue 6, 2012, Pages 453-488

  Franzblau, Scott G ^b   Degroote, Mary Ann ^a   Cho, Sang Hyun ^b   Andries, Koen ^d   Nuermberger, Eric ^c   Orme, Ian M ^a   Mdluli, Khisimuzi ^e   Angulo Barturen, Iñigo ^f   Dick, Thomas ^g   Dartois, Veronique ^h   Lenaerts, Anne J ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d Pharmaceuticals Inc   (Belgium)

^e GLOBAL ALLIANCE FOR TB DRUG DEVELOPMENT   (United States)

^f GLAXOSMITHKLINE   (Spain)

^g NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^h PUBLIC HEALTH RESEARCH INSTITUTE   (United States)

Author keywords

Animal models; Drugs; Efficacy testing; Historic review; In vitro; In vivo; Relapse; Screening methods; Tuberculosis

Indexed keywords

AMIKACIN; AMINO ACID; BEDAQUILINE; CAPREOMYCIN; CLARITHROMYCIN; CLOFAZIMINE; CYCLOSERINE; ECONAZOLE; ERYTHROMYCIN; ETHAMBUTOL; ETHIONAMIDE; GLUCOSE; ISONIAZID; KETOCONAZOLE; LEVOFLOXACIN; LINEZOLID; NITROFURANTOIN; OFLOXACIN; OXYTETRACYCLINE; PALMITIC ACID; PYRAZINAMIDE; RIFAMPICIN; RIFAPENTINE; STREPTOMYCIN; STREPTOVARICIN; THIOACETAZONE; TUBERCULOSTATIC AGENT; UNINDEXED DRUG; VANCOMYCIN; VIOMYCIN;

ARTICLE; BACTERIAL GROWTH; BACTERIUM CULTURE; CELL ASSAY; CLINICAL PROTOCOL; CULTURE MEDIUM; DRUG EFFICACY; DRUG SCREENING; GUINEA PIG; IN VITRO STUDY; IN VIVO STUDY; MINIMUM INHIBITORY CONCENTRATION; MODEL; MYCOBACTERIUM BOVIS; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; TUBERCULOSIS;

ANIMALS; ANTITUBERCULAR AGENTS; BACTERIAL PROTEINS; DISEASE MODELS, ANIMAL; DRUG DESIGN; DRUG EVALUATION, PRECLINICAL; HUMANS; MICE; MYCOBACTERIUM TUBERCULOSIS; TUBERCULOSIS;

EID: 84867334162     PISSN: 14729792     EISSN: 1873281X     Source Type: Journal    
DOI: 10.1016/j.tube.2012.07.003     Document Type: Article

References (257)

1. A.M. Ginsberg Drugs in development for tuberculosis Drugs 70 2010 2201 2214 10.2165/11538170-000000000-00000
2. A.M. Ginsberg Tuberculosis drug development: progress, challenges, and the road ahead Tuberculosis 90 2010 162 167 10.1016/j.tube.2010.03.003
3. E.L. Nuermberger, M.K. Spigelman, and W.W. Yew Current development and future prospects in chemotherapy of tuberculosis Respirology 15 2010 764 778 doi:RES1775
4. D.J. Payne, M.N. Gwynn, D.J. Holmes, and D.L. Pompliano Drugs for bad bugs: confronting the challenges of antibacterial discovery Nat Rev Drug Discov 6 2007 29 40 doi:nrd2201
5. Global Alliance for TB drug development. http://www.tballiance.org/cptr/.
6. E. Nuermberger Using animal models to develop new treatments for tuberculosis Semin Respir Crit Care Med 29 2008 542 551 10.1055/s-0028-1085705
7. Tuberculosis Scientific blueprint for tuberculosis drug development Tuberculosis 81 Suppl. 1 2001 1 52
8. M. Nocard, and E. Roux Sur la culture du bacille de la tuberculose Ann Inst Pasteur 1 1888 19 29
9. A. Hammerschlag Bakteriologisch-chemische Untersuchungen uber Tuberkelbacillen Zentr klin Med 1891 9 18
10. W. Kune Zeitschr F Biol 30 1892 221
11. B. Proskauer, and M. Beck Beitrage zur Ernahrungs-physiologie des Tuberkelbacillus Z Hyg Infectionskrankh 18 1894 128 152
12. P. Armand-Delille, A. Mater, G. Schaeffer, and E. Terroine Culture du bacille de Koch en milieu chimiquement defini Compt Rend Soc Biol 74 1913 272 274
13. E.R. Long The nutrition of acid-fast bacteria Am Rev Tuberc 5 1922 857 869
14. R.J. Dubos, and B.D. Davis Factors affecting the growth of tubercle bacilli in liquid media J Exp Med 83 1946 409 423
15. P.D. Crimm, and V.F. Martos Effects of Amigen and amino acids on the growth of tubercle bacilli Am Rev Tuberc 49 1944 94 104
16. Bernheim F. The effect of salicylate on oxygen uptake of the tubercle bacillus. 1940;92:204.
17. J. Lehman Para-aminosalicylic acid in the treatment of tuberculosis Lancet 250 1946 15 16
18. W. Klip The tuberculostatic action of vitamin D2 Antonie Van Leeuwenhoek 18 1952 217 226
19. A.S. Youmans, and G.P. Youmans The effect of "Tween 80" in vitro on the bacteriostatic activity of twenty compounds for Mycobacterium tuberculosis J Bacteriol 56 1948 245 252
20. M.I. Smith Chemotherapeutic testing in experimental tuberculosis Am Rev Tuberc 56 1947 377 381
21. M.I. Smith Quantitative measurement of Mycobacterium tuberculosis Proc Soc Exp Biol Med 64 1947 36 40
22. G.P. Youmans Test tube evaluation of tuberculostatic agents Am Rev Tuberc 56 1947 376
23. B.D. Davis, and R.J. Dubos The binding of fatty acids by serum albumin, a protective growth factor in bacteriological media J Exp Med 86 1947 215 228
24. A.S. Youmans, and G.P. Youmans Studies on the metabolism of Mycobacterium tuberculosis. IV. The effect of fatty acids on the growth of M. tuberculosis var. hominis J Bacteriol 67 1954 731 733
25. E.M. Bavin, D.J. Drain, M. Seiler, and D.E. Seymour Some further studies on tuberculostatic compounds J Pharm Pharmacol 4 1952 844 855
26. G.L. Hobby, T.F. Lenert, M. Donikian, and D. Pikula The tuberculostatic activity of terramycin Am Rev Tuberc 63 1951 434 440
27. T.H. Sattler, and G.P. Youmans The effect of tween 80, bovine albumin, glycerol, and glucose on the growth of Mycobacterium tuberculosis var. hominis (H37Rv) J Bacteriol 56 1948 235 243
28. J. Lehman On the effect of isomers of para-aminosalicylic acid and related substances on the tuberculostatic effect of PAS Experientia 5 1949 365 367
29. H. Beeuwkes On the use of an egg agar medium in the determination of the resistance of Mycobacterium tuberculosis to streptomycin Antonie Van Leeuwenhoek 16 1950 359 365
30. C. Van Der Stelt, A.J. Voorspuij, and W.T. Nauta Investigation into the tuberculostatic activity of some derivatives of p. amino-benzoic acid Antonie Van Leeuwenhoek 20 1954 285 298
31. J. Gootjes, A.J. Zwart Voorspuij, and W.T. Nauta Investigation into the tuberculostatic activity of some aromatic hydroxy compounds Antonie Van Leeuwenhoek 19 1953 237 244
32. W. Steenken Jr., and E. Wolinsky The tuberculostatic action of terramycin in vitro and in the experimental animal Ann N Y Acad Sci 53 1950 309 318
33. W. Steenken Jr., and E. Wolinsky Effects of antimicrobial agents on the tubercle bacillus and on experimental tuberculosis Am J Med 9 1950 633 653 doi:0002-9343(50)90213-0
34. E.M. Bavin, R.J. Rees, J.M. Robson, M. Seiler, D.E. Seymour, and D. Suddaby The tuberculostatic activity of some thiosemicarbazones J Pharm Pharmacol 2 1950 764 772
35. E. Wolinsky, V. Wetzel, and W. Steenken Jr. Tuberculostatic effect of furacin in vitro and in vivo Proc Soc Exp Biol Med 70 1949 483 487
36. Q.R. Bartz, J. Ehrlich, J.D. Mold, M.A. Penner, and R.M. Smith Viomycin, a new tuberculostatic antibiotic Am Rev Tuberc 63 1951 4 6
37. R. Donovick, G. Rake, and E.O. Titus An approach to a correlation between in vivo and in vitro activities of antitubercular compounds Ann NY Acad Sci 53 1950 50 58
38. N. Muic, D. Sudic, and D. Fles Tuberculostatic activity of some pyrrole-azo-derivatives in vitro Acta Med Iugosl 6 1952 141 153
39. W. Klip, A. Emmerie, and C. Engel The tuberculostatic properties of the unsaponifiable fraction of cod liver oil Antonie Van Leeuwenhoek 18 1952 227 237
40. M.M. Abdel Kader, and O. Zaki Tryptophane as a tuberculostatic agent Experientia 14 1958 455 456
41. Q. Myrvik, and R.S. Weiser A tuberculostatic serum substance possessing lysozyme-like properties Am Rev Tuberc 64 1951 669 674
42. Y. Fujita Studies on antituberculous factors in the low molecular fractions of the sera of various animal species. I. Crude materials and their tuberculostatic effects Acta Tuberc Jpn 10 1960 67 74
43. K.B. Bjornesjo Tuberculostatic factor in normal human urine Am Rev Tuberc 73 1956 967
44. R.J. Dubos A tuberculostatic agent present in animal tissues Am Rev Tuberc 63 1951 119
45. K.B. Bjornesjo On the occurrence of tuberculostatic substances in bovine organ estracts Acta Tuberc Scand 27 1952 134 139
46. W.L. Bloom, P.C. Hudgins, and M.M. Cummings Tuberculostatic substances extracted from normal rat spleen J Infect Dis 92 1953 70 73
47. R.A. Patnode, and P.C. Hudgins Tuberculostatic effect of calf lung fatty acids on human and bovine tubercle bacilli Am Rev Tuberc 75 1957 630 637
48. Q.N. Myrvik, and E. Soto-Figueroa A new tuberculostatic protein isolated from bovine spleen Am Rev Tuberc 78 1958 93 100
49. H.C. Ballon, and A. Guernon Tuberculostatic activity of certain products of growth of penicillin notatum Can Med Assoc J 62 1950 277
50. D.E. Jenkins Mycomycin: a new antibiotic with tuberculostatic properties J Lab Clin Med 36 1950 841 842
51. G.L. Hobby, T.F. Lenert, M. Donikian, and D. Pikula The activity of viomycin against Mycobacterium tuberculosis and other microorganisms in vitro and in vivo Am Rev Tuberc 63 1951 17 24
52. H.F. Lee, E. Sewell, and D. Mervine Study of culture filtrates of pathogenic fungi and yeasts for tuberculostatic properties Am Rev Tuberc 66 1952 623 625
53. D. Yegian, and V. Budd Novobiocin: activity in vitro and in experimental tuberculosis Am Rev Tuberc 76 1957 272 278
54. I. Uesaka, H. Yoshioka, and E. Wakuda On the antibiotic activity of Mycobacteria and Nocardia; preliminary report on a tuberculostatic substance contained in bacteria cell Acta Tuberc Jpn 4 1954 1 6
55. I. Uesaka, H. Yoshioka, and E. Wakuda On the antibiotic activity of mycobacteria. I. The existence of a tuberculostatic substance in the bacterial cell body J Antibiot (Tokyo) 8 1955 1 4
56. G. Middlebrook, Z. Reggiardo, and W.D. Tigertt Automatable radiometric detection of growth of Mycobacterium tuberculosis in selective media Am Rev Respir Dis 115 1977 1066 1069
57. S.H. Siddiqi, J.P. Libonati, and G. Middlebrook Evaluation of rapid radiometric method for drug susceptibility testing of Mycobacterium tuberculosis J Clin Microbiol 13 1981 908 912
58. D.E. Snider Jr., R.C. Good, J.O. Kilburn, L.F. Laskowski Jr., R.H. Lusk, J.J. Marr, Z. Reggiardo, and G. Middlebrook Rapid drug-susceptibility testing of Mycobacterium tuberculosis Am Rev Respir Dis 123 1981 402 406
59. C. Piersimoni, A. Olivieri, L. Benacchio, and C. Scarparo Current perspectives on drug susceptibility testing of Mycobacterium tuberculosis complex: the automated nonradiometric systems J Clin Microbiol 44 2006 20 28 doi:44/1/20
60. T. Primm, and S.G. Franzblau Recent advances in methodologies for the discovery of antimycobacterial drugs Curr Bioact Compd 3 2007 201 208
61. L. Collins, and S.G. Franzblau Microplate alamar blue assay versus BACTEC 460 system for high-throughput screening of compounds against Mycobacterium tuberculosis and Mycobacterium avium Antimicrob Agents Chemother 41 1997 1004 1009
62. T.M. Arain, A.E. Resconi, M.J. Hickey, and C.K. Stover Bioluminescence screening in vitro (Bio-Siv) assays for high-volume antimycobacterial drug discovery Antimicrob Agents Chemother 40 1996 1536 1541
63. L.A. Collins, M.N. Torrero, and S.G. Franzblau Green fluorescent protein reporter microplate assay for high-throughput screening of compounds against Mycobacterium tuberculosis Antimicrob Agents Chemother 42 1998 344 347
64. M. Altaf, C.H. Miller, D.S. Bellows, and R. O'Toole Evaluation of the Mycobacterium smegmatis and BCG models for the discovery of Mycobacterium tuberculosis inhibitors Tuberculosis (Edinb) 90 2010 333 337 doi:S1472-9792(10)00103-4
65. K. Pethe, P.C. Sequeira, S. Agarwalla, K. Rhee, K. Kuhen, W.Y. Phong, V. Patel, D. Beer, J.R. Walker, J. Duraiswamy, J. Jiricek, T.H. Keller, A. Chatterjee, M.P. Tan, M. Ujjini, S.P. Rao, L. Camacho, P. Bifani, P.A. Mak, I. Ma, S.W. Barnes, Z. Chen, D. Plouffe, P. Thayalan, S.H. Ng, M. Au, B.H. Lee, B.H. Tan, S. Ravindran, M. Nanjundappa, X. Lin, A. Goh, S.B. Lakshminarayana, C. Shoen, M. Cynamon, B. Kreiswirth, V. Dartois, E.C. Peters, R. Glynne, S. Brenner, and T. Dick A chemical genetic screen in Mycobacterium tuberculosis identifies carbon-source-dependent growth inhibitors devoid of in vivo efficacy Nat Commun 1 2010 1 8 doi:ncomms1060
66. A.K. Ojha, A.D. Baughn, D. Sambandan, T. Hsu, X. Trivelli, Y. Guerardel, A. Alahari, L. Kremer, W.R. Jacobs Jr., and G.F. Hatfull Growth of Mycobacterium tuberculosis biofilms containing free mycolic acids and harbouring drug-tolerant bacteria Mol Microbiol 69 2008 164 174 doi:MMI6274
67. C. Sala, N. Dhar, R.C. Hartkoorn, M. Zhang, Y.H. Ha, P. Schneider, and S.T. Cole Simple model for testing drugs against nonreplicating Mycobacterium tuberculosis Antimicrob Agents Chemother 54 2010 4150 4158 doi:AAC.00821-10
68. T. Christophe, M. Jackson, H.K. Jeon, D. Fenistein, M. Contreras-Dominguez, J. Kim, A. Genovesio, J.P. Carralot, F. Ewann, E.H. Kim, S.Y. Lee, S. Kang, M.J. Seo, E.J. Park, H. Skovierova, H. Pham, G. Riccardi, J.Y. Nam, L. Marsollier, M. Kempf, M.L. Joly-Guillou, T. Oh, W.K. Shin, Z. No, U. Nehrbass, R. Brosch, S.T. Cole, and P. Brodin High content screening identifies decaprenyl-phosphoribose 2′ epimerase as a target for intracellular antimycobacterial inhibitors PLoS Pathog 5 2009 e1000645 10.1371/journal.ppat.1000645
69. R.S. Wallis, M. Palaci, S. Vinhas, A.G. Hise, F.C. Ribeiro, K. Landen, S.H. Cheon, H.Y. Song, M. Phillips, R. Dietze, and J.J. Ellner A whole blood bactericidal assay for tuberculosis J Infect Dis 183 2001 1300 1303 doi:10.1086/319679
70. E. Janulionis, C. Sofer, H.Y. Song, and R.S. Wallis Lack of activity of orally administered clofazimine against intracellular Mycobacterium tuberculosis in whole-blood culture Antimicrob Agents Chemother 48 2004 3133 3135 10.1128/AAC.48.8.3133-3135.2004
71. R.S. Wallis, W. Jakubiec, M. Mitton-Fry, L. Ladutko, S. Campbell, D. Paige, A. Silvia, and P.F. Miller Rapid evaluation in whole blood culture of regimens for XDR-TB containing PNU-100480 (sutezolid), TMC207, PA-824, SQ109, andpyrazinamide PloS One 7 2012 e30479 10.1371/journal.pone.0030479
72. V. Lorian, and M. Finland In vitro effect of rifampin on mycobacteria Appl Microbiol 17 1969 202 207
73. W.A. Zygmunt Antagonism of D-Cycloserine inhibition of mycobacterial growth by D-Alanine J Bacteriol 85 1963 1217 1220
74. A.J. Lenaerts, V. Gruppo, K.S. Marietta, C.M. Johnson, D.K. Driscoll, N.M. Tompkins, J.D. Rose, R.C. Reynolds, and I.M. Orme Preclinical testing of the nitroimidazopyran PA-824 for activity against Mycobacterium tuberculosis in a series of in vitro and in vivo models Antimicrob Agents Chemother 49 2005 2294 2301 doi:49/6/2294
75. S.H. Cho, S. Warit, B. Wan, C.H. Hwang, G.F. Pauli, and S.G. Franzblau Low-oxygen-recovery assay for high-throughput screening of compounds against nonreplicating Mycobacterium tuberculosis Antimicrob Agents Chemother 51 2007 1380 1385 10.1128/AAC.00055-06
76. M. Gengenbacher, S.P. Rao, K. Pethe, and T. Dick Nutrient-starved, non-replicating Mycobacterium tuberculosis requires respiration, ATP synthase and isocitrate lyase for maintenance of ATP homeostasis and viability Microbiology 156 2010 81 87 10.1099/mic.0.033084-0
77. S. Sulochana, D.A. Mitchison, G. Kubendiren, P. Venkatesan, and C.N. Paramasivan Bactericidal activity of moxifloxacin on exponential and stationary phase cultures of Mycobacterium tuberculosis J Chemother 21 2009 127 134
78. L.P. de Carvalho, G. Lin, X. Jiang, and C. Nathan Nitazoxanide kills replicating and nonreplicating Mycobacterium tuberculosis and evades resistance J Med Chem 52 2009 5789 5792 10.1021/jm9010719
79. N. Andreu, T. Fletcher, N. Krishnan, S. Wiles, and B.D. Robertson Rapid measurement of antituberculosis drug activity in vitro and in macrophages using bioluminescence J Antimicrob Chemother 67 2012 404 414 10.1093/jac/dkr472
80. D. Young Animal models of tuberculosis Eur J Immunol 39 2009 2011 2014 10.1002/eji.200939542
81. A.J. Lenaerts, M.A. Degroote, and I.M. Orme Preclinical testing of new drugs for tuberculosis: current challenges Trends Microbiol 16 2008 48 54 doi:S0966-842X(07)00249-1
82. E.R. Baldwin, S.A. Petroff, and L.S. Gardner Tuberculosis: bacteriology, pathology, and laboratory diagnosis 1927 Lea and Febiger Philadelphia
83. H.J. Corper Studies in the biochemistry and chemotherapy of tuberculosis. XII. The action of sodium thiocyanate in tuberculosis J Infect Dis 16 1915 38 46
84. Schroder G. The treatment of tuberculosis with silicylricinolic-acid ethyl ester (Silogran). 1936;88:248-53.
85. M.A. Soltys, and A.R. Jennings The dissemination of tubercle bacilli in experimental tuberculosis in the guinea pig Am Rev Tuberc 61 1950 399 406
86. W. Feldman Experimental evaluation of antibacterial agents in tuberculosis therapy Irish J Med Sci 1951 505 527
87. G.P. Youmans, and G.W. Raleigh The use of mice in experimental chemotherapy of tuberculosis; the histopathologic assay of chemotherapeutic action J Infect Dis 82 1948 221 225
88. G.W. Raleigh, and G.P. Youmans The use of mice in experimental chemotherapy of tuberculosis; pathology and pathogenesis J Infect Dis 82 1948 205 220
89. G.W. Raleigh, and G.P. Youmans The use of mice in experimental chemotherapy of tuberculosis; rationale and review of the literature J Infect Dis 82 1948 197 204
90. R.M. McCune, F.M. Feldmann, H.P. Lambert, and W. McDermott Microbial persistence. I. The capacity of tubercle bacilli to survive sterilization in mouse tissues J Exp Med 123 1966 445 468
91. R.M. McCune, F.M. Feldmann, and W. McDermott Microbial persistence. II. Characteristics of the sterile state of tubercle bacilli J Exp Med 123 1966 469 486
92. R.M. McCune Jr., W. McDermott, and R. Tompsett The fate of Mycobacterium tuberculosis in mouse tissues as determined by the microbial enumeration technique. II. The conversion of tuberculous infection to the latent state by the administration of pyrazinamide and a companion drug J Exp Med 104 1956 763 802
93. R.M. McCune Jr., and R. Tompsett Fate of Mycobacterium tuberculosis in mouse tissues as determined by the microbial enumeration technique. I. The persistence of drug-susceptible tubercle bacilli in the tissues despite prolonged antimicrobial therapy J Exp Med 104 1956 737 762
94. G.P. Youmans, and E.H. Williston The effect of streptomycin on well-established experimental tuberculosis of mice Proc Soc Exp Biol Med 68 1948 661 664
95. G. Middlebrook, and M.L. Cohn Bacteriology of tuberuclosis: laboratory methods Am J Public Health 48 1958 844 853
96. G. Middlebrook, M.L. Cohn, W.E. Dye, W.F. Russell, and D. Levy Microbiologic procedures of value in tuberculosis Acta Tuberc Scand 38 1960 66 81
97. P. Acred, D.M. Brown, and D. Wright The antitubercular activity of 3-acetylthiopropylene sulphide and 3-(2-furoylthio) propylene sulphide Br J Pharmacol Chemother 15 1960 496 499
98. W.H. Feldman, and H.C. Hinshaw Chemotherapeutic testing in experimental tuberculosis. Suggested outline of laboratory procedures for testing antituberculous substances in experimentally infected animals Am Rev Tuberc 51 1945 582 591
99. A.G. Karlson, J.H. Gainer, and W.H. Feldman The effect of neomycin on tuberculosis in guinea pigs infected with streptomycin-resistant tubercle bacilli Am Rev Tuberc 62 1950 345 352
100. P. Hunter Experimental models in antimicrobial chemotherapy 1986 Academic Press
101. C. Pierce, R.J. Dubos, and G. Middlebrook Infection of mice with Mammalian tubercle bacilli grown in Tween-albumin liquid medium J Exp Med 86 1947 159 174
102. A.C. Woods, and E.L. Burky Studies in experimental ocular tuberculosis. The effect of promin and promizole in experimental ocular tuberculosis in the immune-allergic rabbit Trans Am Ophthalmol Soc 45 1947 170 183
103. A.C. Woods, and E.L. Burky Effect of promin and promizole in experimental ocular tuberculosis in the normal rabbit Arch Ophthalmol 40 1948 1 13
104. J. Francis, A. Spinks, and G.T. Stewart The toxic and antituberculous effects of two thiosemicarbazones and streptomycin in dogs, monkeys, and guineapigs Br J Pharmacol Chemother 5 1950 549 564
105. L.H. Schmidt Studies on the antituberculous activity of ethambutol in monkeys Ann NY Acad Sci 135 1966 747 758
106. T.H. Kim, and G.P. Kubica Long-term preservation and storage of mycobacteria Appl Microbiol 24 1972 311 317
107. G.P. Kubica, T.H. Kim, and F.P. Dunbar Designation of H37Rv as the neotype of Mycobacterium tuberculosis Int J Syst Bacteriol 22 1972 99 106
108. W. Steenken, W.H. Oatway, and S.A. Petroff Biological studies of the tubercle bacillus: Iii. Dissociation and Pathogenicity of the R and S Variants of the human tubercle bacillus (H(37)) J Exp Med 60 1934 515 540
109. Trudeau Institute. Catalog of the Trudeau mycobacterial culture collection.
110. W.H. Feldman Tuberculosis chemotherapy: reminiscence of in vivo research Scand J Respir Dis 50 1969 186 196
111. G.A. Rook, and J.L. Stanford The Koch phenomenon and the immunopathology of tuberculosis Curr Top Microbiol Immunol 215 1996 239 262
112. A. Sakula Centenary of the discovery of the tubercle bacillus Lancet 1 1982 750 doi:S0140-6736(82)92671-X
113. A. Sakula Robert Koch: centenary of the discovery of the tubercle bacillus, 1882 Thorax 37 1982 246 251
114. T. Brock Robert Koch: a life in medicine and bacteriology 1999 American Society of Microbiology
115. W.H. Feldman, H.C. Hinshaw, and A.G. Karlson Frequency of administration of streptomycin; its influence on results of treatment of tuberculosis in guinea pigs Am Rev Tuberc 55 1947 435 443
116. W.H. Feldman, H.C. Hinshaw, and F.C. Mann Studies in streptomycin in tuberculosis; the action of streptomycin in experimental tuberculosis Trans Annu Meet Natl Tuberc Assoc 42 1947 64
117. W.H. Feldman, A.G. Karlson, and H.C. Hinshaw Streptomycin in experimental tuberculosis: the effects in guinea pigs following infection in intravenous inoculation Am Rev Tuberc 56 1947 346 359
118. A.G. Karlson, K.H. Pfuetze, D.T. Carr, W.H. Feldman, and H.C. Hinshaw The effect of combined therapy with streptomycin, para-aminosalicylic acid and promin on the emergence of streptomycin-resistant strains of tubercle bacilli; a preliminary report Proc Staff Meet Mayo Clin 24 1949 85 88
119. A.G. Karlson Streptovaricin: therapeutic effect on guinea pigs infected with tubercle bacilli resistant to streptomycin and to para-aminosalicylic acid Proc Staff Meet Mayo Clin 33 1958 193 196
120. W.H. Feldman, and H.C. Hinshaw Sulfapyridine in experimental tuberculosis Am Rev Tuberc 41 1940 732 750
121. D.G. Smith, and S.A. Waksman Tuberculostatic and tuberculocidal properties of streptomycin J Bacteriol 54 1947 253 261
122. W.H. Feldman, and H.C. Hinshaw Streptomycin; a valuable anti-tuberculosis agent Br Med J 1 1948 87 92
123. P.D. Hart Chemotherapy of tuberculosis; research during the past 100 years Br Med J 2 1946 805 [passim]
124. C.V. Ramakrishnan, A.L. Bhatia, W. Fox, D.A. Mitchison, S. Radhakrishna, J.B. Selkon, T.V. Subbaiah, S. Velu, and J.G. Wallace The virulence in the guinea-pig of tubercle bacilli isolated before treatment from South Indian patients with pulmonary tuberculosis. 3. Virulence related to pretreatment status of disease and to response to chemotherapy Bull World Health Organ 25 1961 323 338
125. T.V. Subbaiah, A.L. Bhatia, E. Geraghty, D.A. Mitchison, S. Radhakrishna, and J.B. Selkon The virulence in the guinea-pig of isoniazid-sensitive tubercle bacilli isolated from South Indian patients before treatment and after three months of chemotherapy Bull World Health Organ 25 1961 759 764
126. J.M. Dickinson, and D.A. Mitchison Experimental investigations of bacteriological mechanisms in short course chemotherapy Bull Int Union Against Tuberc 51 1976 79 86
127. J.M. Dickinson, and D.A. Mitchison Bactericidal activity in vitro and in the guinea-pig of isoniazid, rifampicin and ethambutol Tubercle 57 1976 251 258
128. J.M. Adams, V.A. Kalajan, B.O. Mork, M. Rosenblatt, W.J. Rothrock, and B.J. O'Loughlin Reversal of tuberculin reaction in early tuberculosis Dis Chest 35 1959 348 356
129. S.A. Waksman Tenth anniversary of the discovery of streptomycin, the first chemotherapeutic agent found to be effective against tuberculosis in humans Am Rev Tuberc 70 1954 1 8
130. M. Wainwright Streptomycin: discovery and resultant controversy Hist Philos Life Sci 13 1991 97 124
131. W. McDermott The story of INH J Infect Dis 119 1969 678 683
132. V. Chorine Action de l'amide nicotinique sur les bacilles du genre mycobacterium Compt Rend Hebdomadaires Séances Acad Sci 220 1945 150 151
133. H. Bonfiglioli, and J.M. Prado Effect of isonicotinic acid hydrazide on experimental tuberculosis in the guinea pig Rev Asoc Med Argent 66 1952 376 377
134. F.I. Dessau, R.L. Yeager, F.J. Burger, and J.H. Williams Pyrazinamide (aldinamide) in experimental tuberculosis of the guinea pig Am Rev Tuberc 65 1952 519 522
135. A.G. Karlson, and W.H. Feldman Isoniazid in experimental tuberculosis of guinea pigs infected with tubercle bacilli resistant to streptomycin and to para-aminosalicylic acid Am Rev Tuberc 66 1952 477 485
136. R.M. Nakamura, K. Kanai, and T. Murohashi Effectiveness of capreomycin against experimental tuberculosis of mice and guinea pigs Kekkaku 39 1964 161 165
137. R.J. Dubos The effect of lipids and serum albumin on bacterial growth J Exp Med 85 1947 9 22
138. M.L. Cohn, C.L. Davis, and G. Middlebrook Airborne immunization against tuberculosis Science 128 1958 1282 1283
139. G. Middlebrook An apparatus for airborne infection of mice Proc Soc Exp Biol Med 80 1952 105 110
140. R.J. Basaraba Experimental tuberculosis: the role of comparative pathology in the discovery of improved tuberculosis treatment strategies Tuberculosis (Edinb) 88 Suppl. 1 2008 S35 S47 doi:S1472-9792(08)70035-0
141. G.P. Youmans, and A.S. Youmans The assessment of antituberculous chemotherapeutic activity in mice, using virulent human-type tubercle bacilli Am Rev Tuberc 64 1951 541 550
142. G.P. Youmans, and A.S. Youmans The relation between the size of the infecting dose of tubercle bacilli and the survival time of mice Am Rev Tuberc 64 1951 534 540
143. F. Grumbach, G. Canetti, and J. Grosset Further experiments on long-term chemotherapy of advanced murine tuberculosis, with emphasis on intermittent regimes Tubercle 45 1964 125 135
144. H.F. Lecoeur, P.H. Lagrange, C. Truffot-Pernot, M. Gheorghiu, and J. Grosset Relapses after stopping chemotherapy for experimental tuberculosis in genetically resistant and susceptible strains of mice Clin Exp Immunol 76 1989 458 462
145. J.M. Dickinson, and D.A. Mitchison In vitro and in vivo studies to assess the suitability of antituberculous drugs for use in intermittent chemotherapy regimens Tubercle 49 Suppl. 1968 66 70
146. Mitchison DA. Treatment of tuberculosis. The Mitchell lecture 1979. J Roy Coll Phys Lond;14:91-5.
147. F. Grumbach Experimental basis for the chemotherapy of tuberculosis Antimicrob Agents Chemother 5 1965 1058 1064
148. F. Grumbach, G. Canetti, J. Grosset, and M. le Lirzin Late results of long-term intermittent chemotherapy of advanced, murine tuberculosis: limits of the murine model Tubercle 48 1967 11 26
149. W. McDermott, R.M. McCune Jr., and R. Tompsett Dynamics of antituberculous chemotherapy Am Rev Tuberc 74 1956 100 108
150. R.M. McCune, K. Deuschle, C. Jordahl, R. Des Prez, C. Muschenheim, and W. McDermott The influence of streptovaricin used alone and with isoniazid in an experimental tuberculous infection in animals, and some clinical observations Am Rev Tuberc 75 1957 659 666
151. J.F. Heffernan Proceedings: latest results of East African/British Medical Research Council short course chemotherapy studies Tubercle 56 1975 165
152. D.A. Mitchison, and K.C. Chang Experimental models of tuberculosis: can we trust the mouse? Am J Respir Crit Care Med 180 2009 201 202 doi:180/3/201
153. W.J. Burman, S. Goldberg, J.L. Johnson, G. Muzanye, M. Engle, A.W. Mosher, S. Choudhri, C.L. Daley, S.S. Munsiff, Z. Zhao, A. Vernon, and R.E. Chaisson Moxifloxacin versus ethambutol in the first 2 months of treatment for pulmonary tuberculosis Am J Respir Crit Care Med 174 2006 331 338 doi:200603-360OC
154. S.E. Dorman, J.L. Johnson, S. Goldberg, G. Muzanye, N. Padayatchi, L. Bozeman, C.M. Heilig, J. Bernardo, S. Choudhri, J.H. Grosset, E. Guy, P. Guyadeen, M.C. Leus, G. Maltas, D. Menzies, E.L. Nuermberger, M. Villarino, A. Vernon, and R.E. Chaisson Substitution of moxifloxacin for isoniazid during intensive phase treatment of pulmonary tuberculosis Am J Respir Crit Care Med 180 2009 273 280 doi:200901-0078OC
155. J. Grosset, C. Truffot-Pernot, C. Lacroix, and B. Ji Antagonism between isoniazid and the combination pyrazinamide-rifampin against tuberculosis infection in mice Antimicrob Agents Chemother 36 1992 548 551
156. D. Almeida, E. Nuermberger, R. Tasneen, I. Rosenthal, S. Tyagi, K. Williams, C. Peloquin, and J. Grosset Paradoxical effect of isoniazid on the activity of rifampin-pyrazinamide combination in a mouse model of tuberculosis Antimicrob Agents Chemother 53 2009 4178 4184 doi:10.1128/AAC.00830-09
157. A.M. Lenaerts, S.E. Chase, A.J. Chmielewski, and M.H. Cynamon Evaluation of rifapentine in long-term treatment regimens for tuberculosis in mice Antimicrob Agents Chemother 43 1999 2356 2360
158. W.J. Burman, and R.R. Reves Hepatotoxicity from rifampin plus pyrazinamide: lessons for policymakers and messages for care providers Am Journal Respir Crit Care Med 164 2001 1112 1113
159. T. Zhang, M. Zhang, I.M. Rosenthal, J.H. Grosset, and E.L. Nuermberger Short-course therapy with daily rifapentine in a murine model of latent tuberculosis infection Am J Respir Crit Care Med 180 2009 1151 1157 doi:200905-0795OC
160. A.J. Lenaerts, C.M. Johnson, K.S. Marrieta, V. Gruppo, and I.M. Orme Significant increases in the levels of liver enzymes in mice treated with anti-tuberculosis drugs Int Journal Antimicrob Agents 26 2005 152 158 10.1016/j.ijantimicag.2005.04.011
161. M. Zhang, S.Y. Li, I.M. Rosenthal, D.V. Almeida, Z. Ahmad, P.J. Converse, C.A. Peloquin, E.L. Nuermberger, and J.H. Grosset Treatment of tuberculosis with Rifamycin-containing regimens in immune deficient mice Am J Respir Crit Care Med 2011 10.1164/rccm.201012-201949OC
162. N. Veziris, M. Ibrahim, N. Lounis, K. Andries, and V. Jarlier Sterilizing activity of second-line regimens containing TMC207 in a murine model of tuberculosis PLoS One 6 2011 e17556 10.1371/journal.pone.0017556
163. S. Shang, C.A. Shanley, M.L. Caraway, E.A. Orme, M. Henao-Tamayo, L. Hascall-Dove, D. Ackart, A.J. Lenaerts, R.J. Basaraba, I.M. Orme, and D.J. Ordway Activities of TMC207, rifampin, and pyrazinamide against Mycobacterium tuberculosis infection in guinea pigs Antimicrob Agents Chemother 55 2011 124 131 doi:10.1128/AAC.00978-10
164. M.A. De Groote, J.C. Gilliland, C.L. Wells, E.J. Brooks, L.K. Woolhiser, V. Gruppo, C.A. Peloquin, I.M. Orme, and A.J. Lenaerts Comparative studies evaluating mouse models used for efficacy testing of experimental drugs against Mycobacterium tuberculosis Antimicrob Agents Chemother 55 2011 1237 1247 doi:10.1128/AAC.00595-10
165. Ioerger TR, Feng Y, Ganesula K, Chen X, Dobos KM, Fortune S, Jacobs WR Jr., Mizrahi V, Parish T, Rubin E, Sassetti C, Sacchettini JC. Variation among genome sequences of H37Rv strains of Mycobacterium tuberculosis from multiple laboratories. J Bacteriol;192:3645-53. doi:JB.00166-10.
166. K. Andries, T. Gevers, and N. Lounis Bactericidal potencies of new regimens are not predictive of their sterilizing potencies in a murine model of tuberculosis Antimicrob Agents Chemother 54 2010 4540 4544 10.1128/AAC.00934-10
167. H. Pan, B.S. Yan, M. Rojas, Y.V. Shebzukhov, H. Zhou, L. Kobzik, D.E. Higgins, M.J. Daly, B.R. Bloom, and I. Kramnik Ipr1 gene mediates innate immunity to tuberculosis Nature 434 2005 767 772 10.1038/nature03419
168. J. Harper, C. Skerry, S.L. Davis, R. Tasneen, M. Weir, I. Kramnik, W.R. Bishai, M.G. Pomper, E.L. Nuermberger, and S.K. Jain Mouse model of necrotic tuberculosis granulomas develops hypoxic lesions J Infect Dis 205 2012 595 602 10.1093/infdis/jir786
169. E.R. Driver, G.R. Ryan, D.R. Hoff, S.M. Irwin, R. Basaraba, I. Kramnik, and A.J. Lenaerts Evaluation of mouse model forming necrotic granulomas using C3HeB/FeJ mice, for the testing of M. tuberculosis drugs Antimicrob Agents Chemother 2012
170. J. Sissons, B.S. Yan, A.V. Pichugin, A. Kirby, M.J. Daly, and I. Kramnik Multigenic control of tuberculosis resistance: analysis of a QTL on mouse chromosome 7 and its synergism with sst1 Genes Immun 10 2009 37 46 10.1038/gene.2008.68
171. S.L. Davis, E.L. Nuermberger, P.K. Um, C. Vidal, B. Jedynak, M.G. Pomper, W.R. Bishai, and S.K. Jain Noninvasive pulmonary [18F]-2-fluoro-deoxy-D-glucose positron emission tomography correlates with bactericidal activity of tuberculosis drug treatment Antimicrob Agents Chemother 53 2009 4879 4884 doi:10.1128/AAC.00789-09
172. R.J. Dubos Gordon Wilson lecture: the experimental analysis of tuberculous infections Trans Am Clin Climatol Assoc 58 1946 117 136
173. S.V. Capuano 3rd, D.A. Croix, S. Pawar, A. Zinovik, A. Myers, P.L. Lin, S. Bissel, C. Fuhrman, E. Klein, and J.L. Flynn Experimental Mycobacterium tuberculosis infection of cynomolgus macaques closely resembles the various manifestations of human M. tuberculosis infection Infect Immun 71 2003 5831 5844
174. D.R. Hoff, G.J. Ryan, E.R. Driver, C.C. Ssemakulu, M.A. De Groote, R.J. Basaraba, and A.J. Lenaerts Location of intra- and extracellular M. tuberculosis populations in lungs of mice and guinea pigs during disease progression and after drug treatment PLoS One 6 2011 e17550 10.1371/journal.pone.0017550
175. J. Grosset Mycobacterium tuberculosis in the extracellular compartment: an underestimated adversary Antimicrob Agents Chemother 47 2003 833 836
176. E.L. Nuermberger, T. Yoshimatsu, S. Tyagi, K. Williams, I. Rosenthal, R.J. O'Brien, A.A. Vernon, R.E. Chaisson, W.R. Bishai, and J.H. Grosset Moxifloxacin-containing regimens of reduced duration produce a stable cure in murine tuberculosis Am J Respir Crit Care Med 170 2004 1131 1134 10.1164/rccm.200407-885OC
177. K.N. Adams, K. Takaki, L.E. Connolly, H. Wiedenhoft, K. Winglee, O. Humbert, P.H. Edelstein, C.L. Cosma, and L. Ramakrishnan Drug tolerance in replicating mycobacteria mediated by a macrophage-induced efflux mechanism Cell 145 2011 39 53 10.1016/j.cell.2011.02.022
178. O. Gil, I. Diaz, C. Vilaplana, G. Tapia, J. Diaz, M. Fort, N. Caceres, S. Pinto, J. Cayla, L. Corner, M. Domingo, and P.J. Cardona Granuloma encapsulation is a key factor for containing tuberculosis infection in minipigs PLoS One 5 2010 e10030 10.1371/journal.pone.0010030
179. L.E. Via, P.L. Lin, S.M. Ray, J. Carrillo, S.S. Allen, S.Y. Eum, K. Taylor, E. Klein, U. Manjunatha, J. Gonzales, E.G. Lee, S.K. Park, J.A. Raleigh, S.N. Cho, D.N. McMurray, J.L. Flynn, and C.E. Barry 3rd Tuberculous granulomas are hypoxic in guinea pigs, rabbits, and nonhuman primates Infect Immun 76 2008 2333 2340 doi:IAI.01515-07
180. M.B. Lurie The use of the rabbit in experimental chemotherapy of tuberculosis Ann NY Acad Sci 52 1949 627 636 illust
181. S.E. Dorman, C.L. Hatem, S. Tyagi, K. Aird, J. Lopez-Molina, M.L. Pitt, B.C. Zook, A.M. Dannenberg Jr., W.R. Bishai, and Y.C. Manabe Susceptibility to tuberculosis: clues from studies with inbred and outbred New Zealand White rabbits Infect Immun 72 2004 1700 1705
182. A.M. Dannenberg Jr. Roles of cytotoxic delayed-type hypersensitivity and macrophage-activating cell-mediated immunity in the pathogenesis of tuberculosis Immunobiology 191 1994 461 473
183. A.M. Dannenberg Jr. Pathogenesis of pulmonary Mycobacterium bovis infection: basic principles established by the rabbit model Tuberculosis 81 2001 87 96 doi:10.1054/tube.2000.0260
184. Y.C. Manabe, A.K. Kesavan, J. Lopez-Molina, C.L. Hatem, M. Brooks, R. Fujiwara, K. Hochstein, M.L. Pitt, J. Tufariello, J. Chan, D.N. McMurray, W.R. Bishai, A.M. Dannenberg Jr., and S. Mendez The aerosol rabbit model of TB latency, reactivation and immune reconstitution inflammatory syndrome Tuberculosis (Edinb) 88 2008 187 196 doi:S1472-9792(07)00131-X
185. L. Tsenova, E. Ellison, R. Harbacheuski, A.L. Moreira, N. Kurepina, M.B. Reed, B. Mathema, C.E. Barry 3rd, and G. Kaplan Virulence of selected Mycobacterium tuberculosis clinical isolates in the rabbit model of meningitis is dependent on phenolic glycolipid produced by the bacilli J Infect Dis 192 2005 98 106 doi:10.1086/430614
186. G.G. Nedeltchev, T.R. Raghunand, M.S. Jassal, S. Lun, Q.J. Cheng, and W.R. Bishai Extrapulmonary dissemination of Mycobacterium bovis but not Mycobacterium tuberculosis in a bronchoscopic rabbit model of cavitary tuberculosis Infect Immun 77 2009 598 603 doi:10.1128/IAI.01132-08
187. K.L. Helke, J.L. Mankowski, and Y.C. Manabe Animal models of cavitation in pulmonary tuberculosis Tuberculosis 86 2006 337 348 10.1016/j.tube.2005.09. 001
188. B. Prideaux, V. Dartois, D. Staab, D.M. Weiner, A. Goh, L.E. Via, C.E. Barry 3rd, and M. Stoeckli High-sensitivity MALDI-MRM-MS imaging of moxifloxacin distribution in tuberculosis-infected rabbit lungs and granulomatous lesions Anal Chem 83 2011 2112 2118 doi:10.1021/ac1029049
189. M.C. Kjellsson, L.E. Via, A. Goh, D. Weiner, K.M. Low, S. Kern, G. Pillai, C.E. Barry 3rd, and V. Dartois Pharmacokinetic evaluation of the penetration of antituberculosis agents in rabbit pulmonary lesions Antimicrob Agents Chemother 56 2012 446 457 doi:10.1128/AAC.05208-11
190. M. Manier, M. Reyzer, A. Goh, V. Dartois, L. Via, Cr Barry, and R. Caprioli Reagent precoated targets for rapid in-tissue derivatization of the anti-tuberculosis drug isoniazid followed by MALDI imaging mass spectrometry J Am Soc Mass Spectrom 22 2011 1409 1419
191. A. Singhal, M. Aliouat el, M. Herve, V. Mathys, M. Kiass, C. Creusy, B. Delaire, L. Tsenova, L. Fleurisse, J. Bertout, L. Camacho, D. Foo, H.C. Tay, J.Y. Siew, W. Boukhouchi, M. Romano, B. Mathema, V. Dartois, G. Kaplan, and P. Bifani Experimental tuberculosis in the Wistar rat: a model for protective immunity and control of infection PloS One 6 2011 e18632 10.1371/journal.pone. 0018632
192. R.L. Elwood, S. Wilson, J.C. Blanco, K. Yim, L. Pletneva, B. Nikonenko, R. Samala, S. Joshi, V.G. Hemming, and M. Trucksis The American cotton rat: a novel model for pulmonary tuberculosis Tuberculosis (Edinb) 87 2007 145 154 doi:S1472-9792(06)00086-2
193. I. Sugawara, H. Yamada, and S. Mizuno Pathological and immunological profiles of rat tuberculosis Int J Exp Pathol 85 2004 125 134 10.1111/j.0959-9673.2004.00379.x
194. I. Sugawara, H. Yamada, and S. Mizuno Pulmonary tuberculosis in spontaneously diabetic goto kakizaki rats Tohoku J Exp Med 204 2004 135 145 doi:JST.JSTAGE/tjem/204.135
195. I. Sugawara, H. Yamada, and S. Mizuno Nude rat (F344/N-rnu) tuberculosis Cell Microbiol 8 2006 661 667 doi:CMI658
196. M.B. Gardner, and P.A. Luciw Macaque models of human infectious disease ILAR J 49 2008 220 255
197. C.J. Batten, R. De Rose, K.M. Wilson, M.B. Agy, S. Chea, I. Stratov, D.C. Montefiori, and S.J. Kent Comparative evaluation of simian, simian-human, and human immunodeficiency virus infections in the pigtail macaque (Macaca nemestrina) model AIDS Res Hum Retroviruses 22 2006 580 588 doi:10.1089/aid. 2006.22.580
198. J.L. Flynn Lessons from experimental Mycobacterium tuberculosis infections Microbes Infect 8 2006 1179 1188 doi:S1286-4579(05)00457-0
199. A.J. Lenaerts, D. Hoff, S. Aly, S. Ehlers, K. Andries, L. Cantarero, I.M. Orme, and R.J. Basaraba Location of persisting mycobacteria in a Guinea pig model of tuberculosis revealed by r207910 Antimicrob Agents Chemother 51 2007 3338 3345 doi:10.1128/AAC.00276-07
200. D.A. Mitchison, and A.R. Coates Predictive in vitro models of the sterilizing activity of anti-tuberculosis drugs Curr Pharm Des 10 2004 3285 3295
201. J. Dhillon, D.B. Lowrie, and D.A. Mitchison Mycobacterium tuberculosis from chronic murine infections that grows in liquid but not on solid medium BMC Infect Dis 4 2004 51 doi:1471-2334-4-51
202. N. Lounis, N. Veziris, A. Chauffour, C. Truffot-Pernot, K. Andries, and V. Jarlier Combinations of R207910 with drugs used to treat multidrug-resistant tuberculosis have the potential to shorten treatment duration Antimicrob Agents Chemother 50 2006 3543 3547 doi:AAC.00766-06
203. R. Tasneen, S.Y. Li, C.A. Peloquin, D. Taylor, K.N. Williams, K. Andries, K.E. Mdluli, and E.L. Nuermberger Sterilizing activity of novel TMC207- and PA-824-containing regimens in a murine model of tuberculosis Antimicrob Agents Chemother 55 2011 5485 5492 doi:10.1128/AAC.05293-11
204. D.L. Cohn, B.J. Catlin, K.L. Peterson, F.N. Judson, and J.A. Sbarbaro A 62-dose, 6-month therapy for pulmonary and extrapulmonary tuberculosis. A twice-weekly, directly observed, and cost-effective regimen Ann Int Med 112 1990 407 415
205. S. Srivastava, and T. Gumbo In vitro and in vivo modeling of tuberculosis drugs and its impact on optimization of doses and regimens Curr Pharmaceutical Design 17 2011 2881 2888
206. L.K. Woolhiser, D.R. Hoff, K.S. Marietta, I.M. Orme, and A.J. Lenaerts Testing of experimental compounds in a relapse model of tuberculosis using granulocyte-macrophage colony-stimulating factor gene-disrupted mice Antimicrob Agents Chemother 53 2009 306 308 doi:10.1128/AAC.01346-07
207. J.L. Flynn, M.M. Goldstein, K.J. Triebold, J. Sypek, S. Wolf, and B.R. Bloom IL-12 increases resistance of BALB/c mice to Mycobacterium tuberculosis infection J Immunol 155 1995 2515 2524
208. U.S. Food and Drug Administration http://www.clinicaltrials.gov/ct2/show/ NCT00864383?term=moxifloxacin&rank=1 2010
209. E.L. Nuermberger, T. Yoshimatsu, S. Tyagi, R.J. O'Brien, A.N. Vernon, R.E. Chaisson, W.R. Bishai, and J.H. Grosset Moxifloxacin-containing regimen greatly reduces time to culture conversion in murine tuberculosis Am J Respir Crit Care Med 169 2004 421 426 10.1164/rccm.200310-1380OC
210. M. Ibrahim, C. Truffot-Pernot, K. Andries, V. Jarlier, and N. Veziris Sterilizing activity of R207910 (TMC207)-containing regimens in the murine model of tuberculosis Am Journal Respir Crit Care Med 180 2009 553 557 10.1164/rccm.200807-1152OC
211. I.M. Rosenthal, M. Zhang, D. Almeida, J.H. Grosset, and E.L. Nuermberger Isoniazid or moxifloxacin in rifapentine-based regimens for experimental tuberculosis? Am J Respir Crit Care Med 178 2008 989 993 10.1164/rccm.200807- 1029OC
212. J.M. Dickinson, V.R. Aber, and D.A. Mitchison Bactericidal activity of streptomycin, isoniazid, rifampin, ethambutol, and pyrazinamide alone and in combination against Mycobacterium Tuberculosis Am Rev Respir Dis 116 1977 627 635
213. M.A. De Groote, V. Gruppo, L.K. Woolhiser, I.M. Orme, J.C. Gilliland, and A.J. Lenaerts Importance of confirming data on the in vivo efficacy of novel antibacterial drug regimens against various strains of Mycobacterium tuberculosis Antimicrob Agents Chemother 56 2012 731 738 doi:10.1128/AAC.05701- 11
214. M. Ibrahim, K. Andries, N. Lounis, A. Chauffour, C. Truffot-Pernot, V. Jarlier, and N. Veziris Synergistic activity of R207910 combined with pyrazinamide against murine tuberculosis Antimicrob Agents Chemother 51 2007 1011 1015 10.1128/AAC.00898-06
215. N. Lounis, T. Gevers, J. Van Den Berg, and K. Andries Impact of the interaction of R207910 with rifampin on the treatment of tuberculosis studied in the mouse model Antimicrob Agents Chemother 52 2008 3568 3572 doi:AAC.00566-08
216. I.M. Rosenthal, K. Williams, S. Tyagi, C.A. Peloquin, A.A. Vernon, W.R. Bishai, J.H. Grosset, and E.L. Nuermberger Potent twice-weekly rifapentine-containing regimens in murine tuberculosis Am J Respir Crit Care Med 174 2006 94 101 doi:200602-280OC
217. American type culture collection. www.atcc.org.
218. E.J. Munoz-Elias, J. Timm, T. Botha, W.T. Chan, J.E. Gomez, and J.D. McKinney Replication dynamics of Mycobacterium tuberculosis in chronically infected mice Infect Immun 73 2005 546 551 doi:73/1/546
219. W.P. Gill, N.S. Harik, M.R. Whiddon, R.P. Liao, J.E. Mittler, and D.R. Sherman A replication clock for Mycobacterium tuberculosis Nat Med 15 2009 211 214 doi:nm.1915
220. Z. Ahmad, M.M. Fraig, G.P. Bisson, E.L. Nuermberger, J.H. Grosset, and P.C. Karakousis Dose-dependent activity of pyrazinamide in animal models of intracellular and extracellular tuberculosis infections Antimicrob Agents Chemother 55 2011 1527 1532 10.1128/AAC.01524-10
221. S.Y. Eum, J.H. Kong, B.Y. Jeon, S.N. Cho, J. Kim, L.E. Via, C.E. Barry Iii, and W.J. Koh Metaplastic ossification in the cartilage of the bronchus of a patient with chronic multi-drug resistant tuberculosis: a case report J Med Case Rep 4 2010 156 10.1186/1752-1947-4-156
222. Converse PJ, Eisenach KD, Theus SA, Nuermberger EL, Tyagi S, Ly LH, Geiman DE, Guo H, Nolan ST, Akar NC, Klinkenberg LG, Gupta R, Lun S, Karakousis PC, Lamichhane G, McMurray DN, Grosset JH, Bishai WR. The impact of mouse passaging of Mycobacterium tuberculosis strains prior to virulence testing in the mouse and guinea pig aerosol models. PLoS One;5:e10289. doi:10.1371/journal. pone.0010289.
223. B. Weiner, J. Gomez, T.C. Victor, R.M. Warren, A. Sloutsky, B.B. Plikaytis, J.E. Posey, P.D. van Helden, N.C. Gey van Pittius, M. Koehrsen, P. Sisk, C. Stolte, J. White, S. Gagneux, B. Birren, D. Hung, M. Murray, and J. Galagan Independent large scale duplications in multiple M. tuberculosis lineages overlapping the same genomic region PloS One 7 2012 e26038 10.1371/journal.pone.0026038
224. D. Portevin, S. Gagneux, I. Comas, and D. Young Human macrophage responses to clinical isolates from the Mycobacterium tuberculosis complex discriminate between ancient and modern lineages PLoS Pathog 7 2011 e1001307 10.1371/journal.ppat.1001307
225. S. Homolka, S. Niemann, D.G. Russell, and K.H. Rohde Functional genetic diversity among Mycobacterium tuberculosis complex clinical isolates: delineation of conserved core and lineage-specific transcriptomes during intracellular survival PLoS Pathog 6 2010 e1000988 10.1371/journal.ppat.1000988
226. S. Borrell, and S. Gagneux Strain diversity, epistasis and the evolution of drug resistance in Mycobacterium tuberculosis Clin Microbiol Infect Off Pub Eur Soc Clin Microbiol Infect Dis 17 2011 815 820 10.1111/j.1469-0691.2011. 03556.x
227. S. Gagneux Host-pathogen coevolution in human tuberculosis Philos Trans Roy Soc Lond Ser B Biol Sci 367 2012 850 859 10.1098/rstb.2011.0316
228. S. Gagneux, M.V. Burgos, K. DeRiemer, A. Encisco, S. Munoz, P.C. Hopewell, P.M. Small, and A.S. Pym Impact of bacterial genetics on the transmission of isoniazid-resistant Mycobacterium tuberculosis PLoS Pathog 2 2006 e61 10.1371/journal.ppat.0020061
229. N. Lari, N. Bimbi, L. Rindi, E. Tortoli, and C. Garzelli Genetic diversity of human isolates of Mycobacterium bovis assessed by spoligotyping and Variable Number Tandem Repeat genotyping Infect Genet Evol J Mol Epidemiol Evol Genet Infect Dis 11 2011 175 180 10.1016/j.meegid.2010.09.004
230. S. Gagneux, and P.M. Small Global phylogeography of Mycobacterium tuberculosis and implications for tuberculosis product development Lancet Infect Dis 7 2007 328 337 doi:S1473-3099(07)70108-1
231. S. Gagneux, K. DeRiemer, T. Van, M. Kato-Maeda, B.C. de Jong, S. Narayanan, M. Nicol, S. Niemann, K. Kremer, M.C. Gutierrez, M. Hilty, P.C. Hopewell, and P.M. Small Variable host-pathogen compatibility in Mycobacterium tuberculosis Proc Natl Acad Sci USA 103 2006 2869 2873 10.1073/pnas.0511240103
232. W.J. Burman, E.E. Bliven, L. Cowan, L. Bozeman, P. Nahid, L. Diem, and A. Vernon Relapse associated with active disease caused by Beijing strain of Mycobacterium tuberculosis Emerg Infect Dis 15 2009 1061 1067 10.3201/eid1507.081253
233. P. Nahid, E.E. Bliven, E.Y. Kim, W.R. Mac Kenzie, J.E. Stout, L. Diem, J.L. Johnson, S. Gagneux, P.C. Hopewell, and M. Kato-Maeda Influence of M. tuberculosis lineage variability within a clinical trial for pulmonary tuberculosis PloS One 5 2010 e10753 10.1371/journal.pone.0010753
234. G.S. Palanisamy, N. Duteau, K.D. Eisenach, D.M. Cave, S.A. Theus, B.N. Kreiswirth, R.J. Basaraba, and I.M. Orme Clinical strains of Mycobacterium tuberculosis display a wide range of virulence in guinea pigs Tuberculosis (Edinb) 2009 doi:S1472-9792(09)00009-2
235. A.K. Barczak, P. Domenech, H.I. Boshoff, M.B. Reed, C. Manca, G. Kaplan, and C.E. Barry 3rd In vivo phenotypic dominance in mouse mixed infections with Mycobacterium tuberculosis clinical isolates J Infect Dis 192 2005 600 606 doi:10.1086/432006
236. T. Luo, C. Yang, S. Gagneux, B. Gicquel, J. Mei, and Q. Gao Combination of single nucleotide polymorphism and variable-number Tandem repeats for genotyping a Homogenous population of Mycobacterium tuberculosis Beijing strains in China J Clin Microbiol 50 2012 633 639 10.1128/JCM.05539-11
237. D. Ordway, M. Henao-Tamayo, M. Harton, G. Palanisamy, J. Troudt, C. Shanley, R.J. Basaraba, and I.M. Orme The hypervirulent Mycobacterium tuberculosis strain HN878 induces a potent TH1 response followed by rapid down-regulation J Immunol 179 2007 522 531 doi:179/1/522
238. D.J. Ordway, C.A. Shanley, M.L. Caraway, E.A. Orme, D.S. Bucy, L. Hascall-Dove, M. Henao-Tamayo, M.R. Harton, S. Shang, D. Ackart, S.L. Kraft, A.J. Lenaerts, R.J. Basaraba, and I.M. Orme Evaluation of standard chemotherapy in the guinea pig model of tuberculosis Antimicrob Agents Chemother 54 2010 1820 1833 10.1128/AAC.01521-09
239. A.M. Cooper, G. Kaplan, and K. Derbyshire TB day summit in upstate New York: key issues to address Eur J Immunol 39 2009 1443 1447 10.1002/eji. 200990031
240. D. Ordway, G. Palanisamy, M. Henao-Tamayo, E.E. Smith, C. Shanley, I.M. Orme, and R.J. Basaraba The cellular immune response to Mycobacterium tuberculosis infection in the guinea pig J Immunol 179 2007 2532 2541 doi:179/4/2532
241. C.K. Stover, P. Warrener, D.R. VanDevanter, D.R. Sherman, T.M. Arain, M.H. Langhorne, S.W. Anderson, J.A. Towell, Y. Yuan, D.N. McMurray, B.N. Kreiswirth, C.E. Barry, and W.R. Baker A small-molecule nitroimidazopyran drug candidate for the treatment of tuberculosis Nature 405 2000 962 966 doi:10.1038/35016103
242. B. Kampmann, G.N. Tena, S. Mzazi, B. Eley, D.B. Young, and M. Levin Novel human in vitro system for evaluating antimycobacterial vaccines Infect Immun 72 2004 6401 6407 doi:72/11/6401
243. Kong Y, Yao H, Ren H, Subbian S, Cirillo SL, Sacchettini JC, Rao J, Cirillo JD. Imaging tuberculosis with endogenous beta-lactamase reporter enzyme fluorescence in live mice. Proc Natl Acad Sci USA;107:12239-44. doi:1000643107.
244. Diacon AH, Maritz JS, Venter A, van Helden PD, Andries K, McNeeley DF, Donald PR. Time to detection of the growth of Mycobacterium tuberculosis in MGIT 960 for determining the early bactericidal activity of antituberculosis agents. Eur J Clin Microbiol Infect Dis. doi:10.1007/s10096-010-1043-7.
245. S.R. Pai, J.K. Actor, E. Sepulveda, R.L. Hunter Jr., and C. Jagannath Identification of viable and non-viable Mycobacterium tuberculosis in mouse organs by directed RT-PCR for antigen 85B mRNA Microb Pathog 28 2000 335 342 10.1006/mpat.2000.0353
246. R. Jayaram, S. Gaonkar, P. Kaur, B.L. Suresh, B.N. Mahesh, R. Jayashree, V. Nandi, S. Bharat, R.K. Shandil, E. Kantharaj, and V. Balasubramanian Pharmacokinetics-pharmacodynamics of rifampin in an aerosol infection model of tuberculosis Antimicrob Agents Chemother 47 2003 2118 2124
247. R.K. Shandil, R. Jayaram, P. Kaur, S. Gaonkar, B.L. Suresh, B.N. Mahesh, R. Jayashree, V. Nandi, S. Bharath, and V. Balasubramanian Moxifloxacin, ofloxacin, sparfloxacin, and ciprofloxacin against Mycobacterium tuberculosis: evaluation of in vitro and pharmacodynamic indices that best predict in vivo efficacy Antimicrob Agents Chemother 51 2007 576 582 10.1128/AAC.00414-06
248. A.H. Diacon, R. Dawson, M. Hanekom, K. Narunsky, S.J. Maritz, A. Venter, P.R. Donald, C. van Niekerk, K. Whitney, D.J. Rouse, M.W. Laurenzi, A.M. Ginsberg, and M.K. Spigelman Early bactericidal activity and pharmacokinetics of PA-824 in smear-positive tuberculosis patients Antimicrob Agents Chemother 54 2010 3402 3407 10.1128/AAC.01354-09
249. Ahmad Z, Peloquin CA, Singh RP, Derendorf H, Tyagi S, Ginsberg A, Grosset JH, Nuermberger EL. PA-824 exhibits time-dependent activity in a murine model of tuberculosis. Antimicrob Agents Chemother. doi:AAC.00849-10.
250. R. Rustomjee, A.H. Diacon, J. Allen, A. Venter, C. Reddy, R.F. Patientia, T.C. Mthiyane, T. De Marez, R. van Heeswijk, R. Kerstens, A. Koul, K. De Beule, P.R. Donald, and D.F. McNeeley Early bactericidal activity and pharmacokinetics of the diarylquinoline TMC207 in treatment of pulmonary tuberculosis Antimicrob Agents Chemother 52 2008 2831 2835 doi:AAC.01204-07
251. E. Nuermberger, I. Rosenthal, S. Tyagi, K.N. Williams, D. Almeida, C.A. Peloquin, W.R. Bishai, and J.H. Grosset Combination chemotherapy with the nitroimidazopyran PA-824 and first-line drugs in a murine model of tuberculosis Antimicrob Agents Chemother 50 2006 2621 2625 10.1128/AAC.00451-06
252. D.J. Horne, S.E. Royce, L. Gooze, M. Narita, P.C. Hopewell, P. Nahid, and K.R. Steingart Sputum monitoring during tuberculosis treatment for predicting outcome: systematic review and meta-analysis Lancet Infect Dis 10 2010 387 394 10.1016/S1473-3099(10)70071-2
253. Controlled clinical trial of four short-course regimens of chemotherapy for two durations in the treatment of pulmonary tuberculosis. Second report. Third East African/British Medical Research Council Study Tubercle 61 1980 59 69
254. R.S. Wallis, T.M. Doherty, P. Onyebujoh, M. Vahedi, H. Laang, O. Olesen, S. Parida, and A. Zumla Biomarkers for tuberculosis disease activity, cure, and relapse Lancet Infect Dis 9 2009 162 172 10.1016/S1473-3099(09)70042-8
255. Spigelman M, Woosley R, Gheuens J. New initiative speeds tuberculosis drug development: novel drug regimens become possible in years, not decades. Int J Tuberc Lung Dis;14:663-4.
256. D.G. Hackam Translating animal research into clinical benefit BMJ 334 2007 163 164 doi:334/7586/163
257. R. Atlas Handbook of microbiological media 2004 CRC Press